Characterization of the neurohypophysial hormone gene loci in elephant shark and the Japanese lamprey: origin of the vertebrate neurohypophysial hormone genes

Abstract

Background: Vasopressin and oxytocin are mammalian neurohypophysial hormones with distinct functions. Vasopressin is involved mainly in osmoregulation and oxytocin is involved primarily in parturition and lactation. Jawed vertebrates contain at least one homolog each of vasopressin and oxytocin, whereas only a vasopressin-family hormone, vasotocin, has been identified in jawless vertebrates. The genes encoding vasopressin and oxytocin are closely linked tail-to-tail in eutherian mammals whereas their homologs in chicken, Xenopus and coelacanth (vasotocin and mesotocin) are linked tail-to-head. In contrast, their pufferfish homologs, vasotocin and isotocin, are located on the same strand of DNA with isotocin located upstream of vasotocin and separated by five genes. These differences in the arrangement of the two genes in different bony vertebrate lineages raise questions about their origin and ancestral arrangement. To trace the origin of these genes, we have sequenced BAC clones from the neurohypophysial gene loci in a cartilaginous fish, the elephant shark (Callorhinchus milii), and in a jawless vertebrate, the Japanese lamprey (Lethenteron japonicum). We have also analyzed the neurohypophysial hormone gene locus in an invertebrate chordate, the amphioxus (Branchiostoma floridae).

Neurohormones: oxytocin, vasopressin and related peptides – structure, genes, receptors, and evolution

“…This study was successfully done by the group of Gwee et al (2009). The tail-tohead orientation of the elephant shark vasotocin and oxytocin genes indicates that this was the ancestral state of the two genes soon after the duplication of the vasotocin gene.…”

“…In jawless vertebrates, only a vasotocin gene has been cloned so far. In the study of Gwee et al (2009), the authors sequenced the neurohypophysial gene loci in a cartilaginous fish, the elephant shark, and a jawless vertebrate, the Japanese lamprey. They also characterized this locus in the genome of amphioxus, a cephalochordate.…”

“…The cephalochordates are the most basal group of chordates and the urochordates are the 'sisters' of vertebrates (Putnam et al, 2008). Recently, a whole-genome sequence of a cephalochordate, the amphioxus, has been completed (Putnam et al, 2008;Gwee et al, 2009).…”

“…The close linkage and organization of these genes have been conserved in a coelacanth, Xenopus, and in chicken and opossum genomes, while the oxytocin gene has undergone a local inversion in human and rodent genomes. In contrast to these vertebrates, the neurohypophysial hormone gene locus in pufferfishes has undergone extensive rearrangements (Gwee et al, 2009). The isotocin gene in fugu has been translocated to a position upstream of the vasotocin gene and the two genes are separated by five unrelated genes.…”

“…In the parvocellular PVN, vasopressin gene expression is suppressed by adrenal glucocorticoids as part of a negative-feedback loop, and is upregulated by stress (Ma et al, 1997), while diurnal cues modulate vasopressin gene expression in the suprachiasmatic nucleus (SCN) (Carter and Murphy, 1991;Murphy and Wells, 2003). Abundant and detailed information on the subject can be found in important and prestigious publications (Gainer and Wray, 1994;Acher, 1996;Hoyle, 1999;Gimpl and Fahreholtz, 2001;Gwee et al, 2009). …”